Abstract
Aims
Soil microorganisms play an important role in biogeochemical cycles in terrestrial ecosystems. Increasing nitrogen (N) and phosphorus (P) deposition are likely to regulate microbial growth by altering soil nutrient availability in tropical forests, yet their impacts on microbial community structure and function between primary forests and secondary forests are not well understood.
Methods
To investigate how nutrient availability affects microbial community structure and function in tropical forests, we measured soil phospholipid fatty acids and enzyme activities in a seven-year N and P fertilization experiment in two tropical montane rainforests, China.
Results
In N addition plots, fungal biomass, arbuscular mycorrhizal fungal biomass and fungi to bacteria ratio (F/B) decreased in the secondary forest, but had moderate changes in the primary forest. In P and N plus P addition plots, microbial biomass showed minor changes, but the F/B increased significantly in both forests. However, hydrolytic enzyme activities did not show a significant change in the secondary forest, while they decreased significantly in the primary forest. Microbial P limitation in the primary forest decreased under P addition and N plus P addition.
Conclusions
Our findings suggest inconsistent responses of microbial community structure and enzyme activity to N and P additions in tropical soils depending on forest type.
Similar content being viewed by others
References
Bach CE, Warnock DD, Van Horn DJ, Weintraub MN, Sinsabaugh RL, Allison SD, German DP (2013) Measuring phenol oxidase and peroxidase activities with pyrogallol, l-DOPA, and ABTS: Effect of assay conditions and soil type. Soil Biol Biochem 67:183–191
Báez S, Homeier J (2018) Functional traits determine tree growth and ecosystem productivity of a tropical montane forest: Insights from a long-term nutrient manipulation experiment. Global Change Biol 24:399–409
Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511
Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microbiol Ecol 35:265–278
Brown S, Lugo AE (1990) Tropical secondary forests. J Trop Ecol 6:1–32
Camenzind T, Homeier J, Dietrich K, Hempel S, Hertel D, Krohn A, Leuschner C, Oelmann Y, Olsson PA, Suarez JP, Rillig MC (2016) Opposing effects of nitrogen versus phosphorus additions on mycorrhizal fungal abundance along an elevational gradient in tropical montane forests. Soil Biol Biochem 94:37–47
Camenzind T, Hättenschwiler S, Treseder KK, Lehmann A, Rillig MC (2018) Nutrient limitation of soil microbial processes in tropical forests. Ecol Monogr 88:4–21
Castrillo G, Teixeira PJPL, Paredes SH, Law TF, de Lorenzo L, Feltcher ME, Finkel OM, Breakfield NW, Mieczkowski P, Jones CD, Paz-Ares J, Dangl JL (2017) Root microbiota drive direct integration of phosphate stress and immunity. Nature 543:513–518
Chen H, Gurmesa GA, Zhang W, Zhu X, Zheng M, Mao Q, Zhang T, Mo J (2016) Nitrogen saturation in humid tropical forests after 6 years of nitrogen and phosphorus addition: hypothesis testing. Funct Ecol 30:305–313
Crowther TW, van den Hoogen J, Wan J, Mayes MA, Keiser AD, Mo L, Averill C, Maynard DS (2019) The global soil community and its influence on biogeochemistry. Science 365:eaav0550
Delgado-Baquerizo M, Eldridge DJ, Ochoa V, Gozalo B, Singh BK, Maestre FT (2017) Soil microbial communities drive the resistance of ecosystem multifunctionality to global change in drylands across the globe. Ecol Lett 20:1295–1305
Du E, Zhou Z, Li P, Hu X, Ma Y, Wang W, Zheng C, Zhu J, He J, Fang J (2013) NEECF: a project of nutrient enrichment experiments in China’s forests. J Plant Ecol 6:428–435
Du E, de Vries W, Han W, Liu X, Yan Z, Jiang Y (2016) Imbalanced phosphorus and nitrogen deposition in China’s forests. Atmos Chem Phys 16:8571–8579
Du E, Fenn M, de Vries W, Ok Y (2019) Atmospheric nitrogen deposition to global forests: Status, impacts and management options. Environ Pollut 250:1044–1048
Fang J, Li Y, Zhu B, Liu G, Zhou G (2004) Community structures and species richness is the montane rain forest of Jianfengling, Hainan Island, China. Biodivers Sci 12:29–43
Fanin N, Fromin N, Buatois B, Hattenschwiler S (2013) An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant littermicrobe system. Ecol Lett 16:764–772
Fanin N, Hättenschwiler S, Schimann H, Fromin N (2015) Interactive effects of C, N and P fertilization on soil microbial community structure and function in an Amazonian rain forest. Funct Ecol 29:140–150
Feng J, Zhu B (2019) A global meta-analysis of soil respiration and its components in response to phosphorus addition. Soil Biol Biochem 135:38–47
Feng C, Ma Y, Jin X, Wang Z, Fu S, Chen H (2019) Soil enzyme activities increase following restoration of degraded subtropical forests. Geoderma 351:180–187
Frostegård Å, Tunlid A, Bååth E (2011) Use and misuse of PLFA measurements in soils. Soil Biol Biochem 43:1621–1625
Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vöosmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226
German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397
Hall SJ, Matson PA (1999) Nitrogen oxide emissions after nitrogen additions in tropical forests. Nature 400:152–155
Han Y, Feng J, Han M, Zhu B (2020) Responses of arbuscular mycorrhizal fungi to nitrogen addition: a meta-analysis. Glob Change Biol 00:1–13. https://doi.org/10.1111/gcb.15369
Hietz P, Turner BL, Wanek W, Richter A, Nock CA, Wright SJ (2011) Long-term change in the nitrogen cycle of tropical forests. Science 334:664–666
Högberg MN, Högberg P, Myrold D (2007) Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia 150:590–601
ITTO (2002) Guidelines for the restoration, management and rehabilitation of degraded and secondary tropical forests. International Tropical Timber Organization, Yokohama
Jiang L, Tian D, Ma S, Zhou X, Xu L, Zhu J, Jing X, Zheng C, Shen H, Zhou Z, Li Y, Zhu B, Fang J (2018) The response of tree growth to nitrogen and phosphorus additions in a tropical montane rainforest. Sci Total Environ 618:1064–1070
Jing X, Chen X, Tang M, Ding Z, Jiang L, Li P, Ma S, Tian D, Xu L, Zhu J, Ji C, Shen H, Zheng C, Fang J, Zhu B (2017) Nitrogen deposition has minor effect on soil extracellular enzyme activities in six Chinese forests. Sci Total Environ 607–608:806–815
Jing X, Chen X, Fang J, Ji C, Shen H, Zheng C, Zhu B (2020) Soil microbial carbon and nutrient constraints are driven more by climate and soil physicochemical properties than by nutrient addition in forest ecosystems. Soil Biol Biochem 141:107657
Kramer C, Gleixner G (2008) Soil organic matter in soil depth profiles: distinct carbon preferences of microbial groups during carbon transformation. Soil Biol Biochem 40:425–433
Krashevska V, Maraun M, Ruess L, Scheu S (2010) Carbon and nutrient limitation of soil microorganisms and microbial grazers in a tropical montane rain forest. Oikos 119:1020–1028
Krashevska V, Sandmann D, Maraun M, Scheu S (2014) Moderate changes in nutrient input alter tropical microbial and protist communities and belowground linkages. ISME J 8:1126–1134
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379
Li J, Li Z, Wang F, Zou B, Chen Y, Zhao J, Mo Q, Li Y, Li X, Xia H (2015) Effects of nitrogen and phosphorus addition on soil microbial community in a secondary tropical forest of China. Biol Fertil Soils 51:207–215
Li P, Shen C, Jiang L, Feng Z, Fang J (2019) Difference in soil bacterial community composition depends on forest type rather than nitrogen and phosphorus additions in tropical montane rainforests. Biol Fertil Soils 55:313–323
Liu L, Gundersen P, Zhang T, Mo J (2012) Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biol Biochem 44:31–38
Liu L, Gundersen P, Zhang W, Zhang T, Chen H, Mo J (2015) Effects of nitrogen and phosphorus additions on soil microbial biomass and community structure in two reforested tropical forests. Sci Rep 5:14378
Lu M, Hedin LO (2019) Global plant–symbiont organization and emergence of biogeochemical cycles resolved by evolution-based trait modelling. Nat Ecol Evol 3:239–250
Lu X, Mao Q, Gilliam FS, Luo Y, Mo J (2014) Nitrogen deposition contributes to soil acidification in tropical ecosystems. Global Change Biol 20:3790–3801
Ma S, Chen G, Tian D, Du E, Xiao W, Jiang L, Zhou Z, Zhu J, He H, Zhu B, Fang J (2020) Effects of seven-year nitrogen and phosphorus additions on soil microbial community structures and residues in a tropical forest in Hainan Island, China. Geoderma 361:114034
Ma S, Chen G, Du E, Tian D, Xing A, Shen H, Ji C, Zheng C, Zhu J, Zhu J, Huang H, He H, Zhu B, Fang J (2021) Effects of nitrogen addition on microbial residues and their contribution to soil organic carbon in China’s forests from tropical to boreal zone. Environ Pollut 268:115941. https://doi.org/10.1016/j.envpol.2020.115941
Martin PA, Newton AC, Bullock LM (2013) Carbon pools recover more quickly than plant biodiversity in tropical secondary forests. Proc R Soc B Biol Sci 280:2013–2236
Mayor JR, Wright SJ, Turner BL (2014) Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forest. J Ecol 102:36–44
Moorhead DL, Rinkes ZL, Sinsabaugh RL, Weintraub MN (2013) Dynamic relationships between microbial biomass, respiration, inorganic nutrients and enzyme activities: informing enzyme-based decomposition models. Front Microbiol 4:223
Mueller RC, Paula FS, Mirza BS, Rodrigues JL, Nüsslein K, Bohannan B (2014) Links between plant and fungal communities across a deforestation chronosequence in the Amazon rainforest. ISME J 8:1548–1550
Peng Y, Chen GS, Chen GT, Li S, Peng TC, Qiu XR, Luo J, Yang SS, Hu TX, Hu HL, Xu ZF, Liu L, Tang Y, Tu LH (2017) Soil biochemical responses to nitrogen addition in a secondary evergreen broad-leaved forest ecosystem. Sci Rep 7:2783
Pinheiro J, Bates D, DebRoy S, Sarkar D (2014) R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package version 3.1–118. R Foundation for Statistical Computing, Vienna
Plassard C, Dell B (2010) Phosphorus nutrition of mycorrhizal trees. Tree Physiol 30:1129–1139
R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Schermelleh-Engel K, Moosbrugger H, Müller H (2003) Evaluating the fit of structural equation models: tests of significance and descriptive goodness-of-fit measures. Meth Psychol Res 8:23–74
Sheldrake M, Rosenstock NP, Mangan S, Revillini D, Sayer EJ, Olsson PA, Verbruggen E, Tanner EV, Turner BL, Wright SJ (2018) Responses of arbuscular mycorrhizal fungi to long-term inorganic and organic nutrient addition in a lowland tropical forest. ISME J 12:2433–2445
Sinsabaugh RL, Moorhead DL (1994) Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition. Soil Biol Biochem 26:1305–1311
Tang W, Chen D, Phillips OL, Liu X, Zhou Z, Li Y, Xi D, Zhu F, Fang J, Zhang L, Lin M, Wu J, Fang Y (2018) Effects of long-term increased N deposition on tropical montane forest soil N2 and N2O emissions. Soil Biol Biochem 126:194–203
Tian D, Jiang L, Ma S, Fang W, Schmid B, Xu L, Zhu J, Li P, Losapio G, Jing X, Zheng C, Shen H, Xu X, Zhu B, Fang J (2017) Effects of nitrogen deposition on soil microbial communities in temperate and subtropical forests in China. Sci Total Environ 607–608:1367–1375
Turner BL, Wright SJ (2014) The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117:115–130
Turner BL, Brenes-Arguedas T, Condit R (2018) Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555:367–370
van der Heijden MGA, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15
Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19
Wang R, Balkanski Y, Boucher O, Ciais P, Peñuelas J, Tao S (2015) Significant contribution of combustion-related emissions to the atmospheric phosphorus budget. Nat Geosci 8:48–54
Wang A, Zhu W, Gundersen P, Phillips OL, Chen D, Fang Y (2018a) Fates of atmospheric deposited nitrogen in an Asian tropical primary forest. For Ecol Manag 411:213–222
Wang C, Lu X, Mori T, Mao Q, Zhou K, Zhou G, Nie Y, Mo J (2018b) Responses of soil microbial community to continuous experimental nitrogen additions for 13 years in a nitrogen-rich tropical forest. Soil Biol Biochem 121:103–112
Wright SJ (2019) Plant responses to nutrient addition experiments conducted in tropical forests. Ecol Monog 89:e01382
Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EV, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:1616–1625
Wright SJ, Turner BL, Yavitt JB, Harms KE, Kaspari M, Tanner EV, Bujan J, Griffin EA, Mayor JR, Pasquini SC (2018) Plant responses to fertilization experiments in lowland, species-rich, tropical forests. Ecology 99:1129–1138
Xiao W, Chen X, Jing X, Zhu B (2018) A meta-analysis of soil extracellular enzyme activities in response to global change. Soil Biol Biochem 123:21–32
Xu H, Li Y, Luo T, Lin M, Chen D, Mo J, Luo W, Hong X, Jiang Z (2009) Community structure characteristics of tropical montane rain forests with different regeneration types in Jianfengling. Sci Sil Sin 45:14–20
Yokoyama D, Imai N, Kitayama K (2017) Effects of nitrogen and phosphorus fertilization on the activities of four different classes of fine-root and soil phosphatases in Bornean tropical rain forests. Plant Soil 416:463–476
Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Peñuelas J, Richter A, Sardans J, Wanek W (2015) The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecol Monog 85:133–155
Zhang T, Chen HYH, Ruan H (2018) Global negative effects of nitrogen deposition on soil microbes. ISME J 12:1817–1825
Zhou Z (2013) Effects of nitrogen and phosphorus additions on carbon cycling of tropical mountain rainforests in Hainan island, China. Peking University, Beijing
Zhou Z, Jiang L, Du E, Hu H, Li Y, Chen D, Fang J (2013) Temperature and substrate availability regulate soil respiration in the tropical mountain rainforests, Hainan Island, China. J Plant Ecol 6:325–334
Zhou Z, Wang C, Zheng M, Jiang L, Luo Y (2017) Patterns and mechanisms of responses by soil microbial communities to nitrogen addition. Soil Biol Biochem 115:433–441
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31988102), the National Key Research and Development Program of China (2017YFC0503906) and the China Postdoctoral Science Foundation (2018M631247). We thank Anwar Eziz, Xin Jing and Zeyuan Li for their helpful suggestions for data analyses and a friendly review of the manuscript. We also thank the anonymous reviewers and the handling editor for their constructive comments that improved this manuscript. The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Jeff R. Powell.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
ESM 1
(DOCX 1.65 MB)
Rights and permissions
About this article
Cite this article
Ma, S., Chen, G., Tang, W. et al. Inconsistent responses of soil microbial community structure and enzyme activity to nitrogen and phosphorus additions in two tropical forests. Plant Soil 460, 453–468 (2021). https://doi.org/10.1007/s11104-020-04805-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-020-04805-9